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SUMMARY: Soil water uptake by roots is a key component of plant water homeostasis contributing to plant growth and survival under ever‐changing environmental conditions. The water transport capacity of roots (root hydraulic conductivity; Lpr) is mostly contributed by finely regulated Plasma membrane Intrinsic Protein (PIP) aquaporins. In this study, we used natural variation of Arabidopsis for the identification of quantitative trait loci (QTLs) contributing to Lpr. Using recombinant lines from a biparental cross (Cvi‐0 x Col‐0), we show that the gene encoding class 2 Sucrose‐Non‐Fermenting Protein kinase 2.4 (SnRK2.4) in Col‐0 contributes to >30% of Lpr by enhancing aquaporin‐dependent water transport. At variance with the inactive and possibly unstable Cvi‐0 SnRK2.4 form, the Col‐0 form interacts with and phosphorylates the prototypal PIP2;1 aquaporin at Ser121 and stimulates its water transport activity upon coexpression in Xenopus oocytes and yeast cells. Activation of PIP2;1 by Col‐0 SnRK2.4 in yeast also requires its protein kinase activity and can be counteracted by clade A Protein Phosphatases 2C. SnRK2.4 shows all hallmarks to be part of core abscisic acid (ABA) signaling modules. Yet, long‐term (>3 h) inhibition of Lpr by ABA possibly involves a SnRK2.4‐independent inhibition of PIP2;1. SnRK2.4 also promotes stomatal aperture and ABA‐induced inhibition of primary root growth. The study identifies a key component of Lpr and sheds new light on the functional overlap and specificity of SnRK2.4 with respect to other ABA‐dependent or independent SnRK2s. [ABSTRACT FROM AUTHOR]